William D. Hamilton

The genetical evolution of social behaviour. I.

Abstract A genetical mathematical model is described which allows for interactions between relatives on one anothers fitness. Making use of Wrights Coefficient of Relationship as the measure of the proportion of replica genes in a relative, a quantity is found which incorporates the maximizing property of Darwinian fitness. This quantity is named “inclusive fitness”. Species following the model should tend to evolve behaviour such that each organism appears to be attempting to maximize its inclusive fitness. This implies a limited restraint on selfish competitive behaviour and possibility of limited self-sacrifices. Special cases of the model are used to show (a) that selection in the social situations newly covered tends to be slower than classical selection, (b) how in populations of rather non-dispersive organisms the model may apply to genes affecting dispersion, and (c) how it may apply approximately to competition between relatives, for example, within sibships. Some artificialities of the model are discussed.

Geometry for the Selfish Herd

Abstract This paper presents an antithesis to the view that gregarious behaviour is evolved through benefits to the population or species. Following Galton (1871) and Williams (1964) gregarious behaviour is considered as a form of cover-seeking in which each animal tries to reduce its chance of being caught by a predator. It is easy to see how pruning of marginal individuals can maintain centripetal instincts in already gregarious species; some evidence that marginal pruning actually occurs is summarized. Besides this, simply defined models are used to show that even in non-gregarious species selection is likely to favour individuals who stay close to others. Although not universal or unipotent, cover-seeking is a widespread and important element in animal aggregation, as the literature shows. Neglect of the idea has probably followed from a general disbelief that evolution can be dysgenic for a species. Nevertheless, selection theory provides no support for such disbelief in the case of species with outbreeding or unsubdivided populations. The model for two dimensions involves a complex problem in geometrical probability which has relevance also in metallurgy and communication science. Some empirical data on this, gathered from random number plots, is presented as of possible heuristic value.

The Genetical Evolution of Social Behaviour. II

Grounds for thinking that the model described in the previous paper can be used to support general biological principles of social evolution are briefly discussed. Two principles are presented, the first concerning the evolution of social behaviour in general and the second the evolution of social discrimination. Some tentative evidence is given. More general application of the theory in biology is then discussed, particular attention being given to cases where the indicated interpretation differs from previous views and to cases which appear anomalous. A hypothesis is outlined concerning social evolution in the Hymenoptera; but the evidence that at present exists is found somewhat contrary on certain points. Other subjects considered include warning behaviour, the evolution of distasteful properties in insects, clones of cells and clones of zooids as contrasted with other types of colonies, the confinement of parental care to true offspring in birds and insects, fights, the behaviour of parasitoid insect larvae within a host, parental care in connection with monogyny and monandry and multi-ovulate ovaries in plants in connection with wind and insect pollination.

The moulding of senescence by natural selection.

Abstract The consequences to fitness of several types of small age-specific effects on mortality are formulated mathematically. An effect of given form always has a larger consequence, or at least one as large, when it occurs earlier. By reference to a model in which mortality is constant it is shown that this implication cannot be avoided by any conceivable organism. A basis for the theory that senescence is an inevitable outcome of evolution is thus established. The simple theory cannot explain specially high infant mortalities. Fishers “reproductive value”, the form of which gave rise to an erroneous opinion on this point, is shown to be not directly relevant to the situation. Infant mortality may evolve when the early death of one infant makes more likely the creation or survival of a close relative. Similarly, post-reproductive life-spans may evolve when the old animal still benefits its younger relatives. The model shows that higher fertility will be a primary factor leading to the evolution of higher rates of senescence unless the resulting extra mortality is confined to the immature period. Some more general analytical notes on the consequences of modifications to the reproductive schedule are given. Applications to species with populations in continual fluctuation are briefly discussed. Such species apart, it is argued that general stationarity of population can be assumed, in which case the measurement of consequences to fitness in terms of consequences to numerical expectation of offspring is justified. All the age-functions discussed are illustrated by graphs derived from the life-table of the Taiwanese about 1906, and the method of computation is shown.

Sex versus non-sex versus parasite

Pressure of parasites that are short-lived and rapid-evolving compared to the hosts they attack could be an evolutionary factor sufficiently general to account for sex wherever it exists. To be such a factor, parasites must show virulences specific to differing genotypes. Models are set up on this basis (one-locus diploid-selection and two-locus haploid-selection) in which the rapid demographic reactivity of parasite strains to abundance of susceptible hosts becomes represented in a single frequency-dependent fitness function which applies to every host genotype. It is shown that with frequency dependence sufficiently intense such models generate cycles, and that in certain states of cycling sexual species easily obtain higher long-term geometric mean fitness than any competing monotypic asexual species or mixture of such. In the successful cycle of the two-locus model, it is seen that both population size and gene frequencies may be steady while only oscillating linkage disequilibrium reflects the intense selection by parasites. High levels of recombination work best. Fecundity in the models can be low and no incidence of competition of siblings or other relatives is required.

Dispersal in stable habitats

Simple mathematical models show that adaptations for achieving dispersal retain great importance even in uniform and predictable environments. A parent organism is expected to try to enter a high fraction of its propagules into competition for sites away from its own immediate locality even when mortality to such dispersing propagules is extremely high. The models incidentally provide a case where the evolutionarily stable dispersal strategy for individuals is suboptimal for the population as a whole.

Evolutionarily stable dispersal strategies

Abstract Using the idea that life-history parameters are subject to natural selection and should approach values that are stable optima, with the population immune to invasion by mutant individuals, we derive an analytic expression for the evolutionarily stable dispersal rate in a stochastic island model with random site extinction. The results provide interesting contrasts between three different optimization criteria: species survival, individual fitness and gene fitness. We also consider the effects of sexual reproduction, and of localized migration (stepping-stone structure).

Low nutritive quality as defense against herbivores

Abstract Contrary to a widespread assumption in the literature on plant-herbivore interactions, individual plants do not necessarily benefit by possessing traits which lower herbivore fitness. In particular, genes conferring lowered nutritive quality could even increase herbivore damage under certain circumstances. Three special sets of conditions are outlined in which low nutritive quality would lower herbivore-induced damage to an individual plant. These sets are far from exhaustive. It is concluded that the adaptiveness of lowered nutritive quality in herbivore defense is widely possible but in no case demonstrated.

Autumn tree colours as a handicap signal.

Many species of deciduous trees display striking colour changes in autumn. Here, we present a functional hypothesis: bright autumn coloration serves as an honest signal of defensive commitment against autumn colonizing insect pests. According to this hypothesis, individuals within a signalling species show variation in the expression of autumn coloration, with defensively committed trees producing a more intense display. Insects are expected to be averse to the brightest tree individuals and, hence, preferentially colonize the least defensive hosts. We predicted that tree species suffering greater insect damage would, on average, invest more in autumn–colour signalling than less troubled species. Here, we show that autumn coloration is stronger in species facing a high diversity of damaging specialist aphids. Aphids are likely to be an important group of signal receivers because they are choosy, damaging and use colour cues in host selection. In the light of further aspects of insect and tree biology, these results support the notion that bright autumn colours are expensive handicap signals revealing the defensive commitment of individual trees to autumn colonizing insect pests.

Cytoplasmic Fusion and the Nature of Sexes

Binary mating types are proposed to arise in a three-stage process through selection of nuclear genes to minimize cytoplasmic gene conflict at the time of gamete fusion. In support of this view we argue that: (i) in systems with fusion of gametes, the mating type genes are typically binary and regulate cytoplasmic inheritance; (ii) binary sexes have evolved several times independently associated with fusion, although at least twice binary types have been lost, associated with a loss of fusion; further, in accordance with the theory are findings for isogamous species that (iii) close inbreeding may correlate with less than two sexes and biparental inheritance of cytoplasmic genes; and (iv) species with more than two sexes may have uniparental inheritance of cytoplasmic genes, be rare and be afflicted by deleterious cytoplasmic genes which attempt to pervert normal cytoplasmic genetics. Such facts and their rationale support a new and unified definition of sexes based on the control of the inheritance of cytoplasmic genes. For the common cases, the male sex is that which resigns attempts to contribute cytoplasmic genes to the next generation. We differentiate between sexes and the incompatibility types of ciliates, basidiomycetes, some angiosperms and a few other organisms which are independent of organelle contribution.